Multi-omics profiling reveals the rhizosphere microecological shifts in the first-cropping Rehmannia glutinosa as potential early triggers for continuous cropping obstacles

The continuous cropping obstacle severely constrains the sustainable production of Rehmannia glutinosa , a geo-authentic medicinal herb cultivated within a limited authentic region. Although autotoxins and microbial dysbiosis have long been implicated, how the first cropping season progressively reshapes the rhizosphere environment remains unclear. This study used an integrated multi-omics approach combining untargeted metabolomics and amplicon sequencing to characterize rhizosphere metabolite–microbiome dynamics during the growing season in first-year R. glutinosa fields. We observed a two-phase accumulation pattern of candidate allelochemicals, including an early and persistent enrichment of phenolic acids (e.g., sinapic acid, caffeic acid) and jasmonates, followed by a late-season pulse of defensive metabolites (e.g., catalpol, coumarin) at harvest. These metabolic shifts were accompanied by a progressive restructuring of the rhizosphere microbiome. In particular, genera containing known plant pathogens (e.g., Plectosphaerella , Albifimbria ) across the season, became increasingly enriched over the season, together with a shift in the soil food web toward a more fungal-dominated energy channel inferred from nematode trophic composition. At the same time, several Actinobacteria with reported antagonistic or degradative capacities, including Streptomyces and Lentzea , were also enriched in the rhizosphere. Integrative analyses further revealed strong associations between specific candidate allelochemicals and the enriched fungal and bacterial taxa. Together, these results indicate that the first cropping season can already generate a rhizosphere legacy characterized by the co-accumulation of defense-related metabolites and microbial groups associated with both pathogen pressure and potential microbial buffering. This early rhizosphere reprogramming may contribute to soil conditions that increase the risk of replant failure in subsequent cycles, and provides a conceptual basis for developing targeted strategies to mitigate continuous cropping obstacles. • Multi-omics resolved first-season rhizosphere dynamic systems in R. glutinosa . • Two-phase allelochemical accumulation marked rhizosphere reprogramming. • Pathogen enrichment and fungal food-web shifts indicated replant risk.